Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation

doi:10.1186/s12943-019-1094-z

. 2019 Nov 13;18(1):158.

doi: 10.1186/s12943-019-1094-z.

Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation

Feng Yang¹, Anpei Hu¹, Dan Li¹, Jianqun Wang¹, Yanhua Guo¹, Yang Liu¹, Hongjun Li², Yajun Chen², Xiaojing Wang³, Kai Huang³, Liduan Zheng^{4

5}, Qiangsong Tong^{6

7}

Affiliations

¹ Department of Pediatric Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
² Department of Pathology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
³ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
⁴ Department of Pathology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. ld_zheng@hotmail.com.
⁵ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. ld_zheng@hotmail.com.
⁶ Department of Pediatric Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. qs_tong@hotmail.com.
⁷ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. qs_tong@hotmail.com.

PMID: 31718709
PMCID: PMC6852727
DOI: 10.1186/s12943-019-1094-z

Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation

Feng Yang et al. Mol Cancer. 2019.

. 2019 Nov 13;18(1):158.

doi: 10.1186/s12943-019-1094-z.

Authors

Feng Yang¹, Anpei Hu¹, Dan Li¹, Jianqun Wang¹, Yanhua Guo¹, Yang Liu¹, Hongjun Li², Yajun Chen², Xiaojing Wang³, Kai Huang³, Liduan Zheng^{4

5}, Qiangsong Tong^{6

7}

Affiliations

¹ Department of Pediatric Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
² Department of Pathology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
³ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China.
⁴ Department of Pathology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. ld_zheng@hotmail.com.
⁵ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. ld_zheng@hotmail.com.
⁶ Department of Pediatric Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. qs_tong@hotmail.com.
⁷ Clinical Center of Human Genomic Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan, Hubei Province, 430022, People's Republic of China. qs_tong@hotmail.com.

PMID: 31718709
PMCID: PMC6852727
DOI: 10.1186/s12943-019-1094-z

Erratum in

Correction: Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation.
Yang F, Hu A, Li D, Wang J, Guo Y, Liu Y, Li H, Chen Y, Wang X, Huang K, Zheng L, Tong Q. Yang F, et al. Mol Cancer. 2023 Sep 20;22(1):155. doi: 10.1186/s12943-023-01862-3. Mol Cancer. 2023. PMID: 37730600 Free PMC article. No abstract available.

Abstract

Background: Circular RNAs (circRNAs), a subclass of non-coding RNAs, play essential roles in tumorigenesis and aggressiveness. Our previous study has identified that circAGO2 drives gastric cancer progression through activating human antigen R (HuR), a protein stabilizing AU-rich element-containing mRNAs. However, the functions and underlying mechanisms of circRNAs derived from HuR in gastric cancer progression remain elusive.

Methods: CircRNAs derived from HuR were detected by real-time quantitative RT-PCR and validated by Sanger sequencing. Biotin-labeled RNA pull-down, mass spectrometry, RNA immunoprecipitation, RNA electrophoretic mobility shift, and in vitro binding assays were applied to identify proteins interacting with circRNA. Gene expression regulation was observed by chromatin immunoprecipitation, dual-luciferase assay, real-time quantitative RT-PCR, and western blot assays. Gain- and loss-of-function studies were performed to observe the impacts of circRNA and its protein partner on the growth, invasion, and metastasis of gastric cancer cells in vitro and in vivo.

Results: Circ-HuR (hsa_circ_0049027) was predominantly detected in the nucleus, and was down-regulated in gastric cancer tissues and cell lines. Ectopic expression of circ-HuR suppressed the growth, invasion, and metastasis of gastric cancer cells in vitro and in vivo. Mechanistically, circ-HuR interacted with CCHC-type zinc finger nucleic acid binding protein (CNBP), and subsequently restrained its binding to HuR promoter, resulting in down-regulation of HuR and repression of tumor progression.

Conclusions: Circ-HuR serves as a tumor suppressor to inhibit CNBP-facilitated HuR expression and gastric cancer progression, indicating a potential therapeutic target for gastric cancer.

Keywords: CCHC-type zinc finger nucleic acid binding protein; Circular RNAs; Gastric cancer; Human antigen R.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

**Fig. 1**
*Circ-HuR* is down-regulated and decreases *HuR* expression in gastric cancer. a RT-PCR assay with divergent primers indicating the detection of three circRNAs derived from *HuR* in AGS cells. b PCR assay with divergent and convergent primers showing the amplification of circRNAs from cDNA or genomic DNA (gDNA) of gastric cancer cell lines, while β-actin was used as a negative control. c Schematic illustration indicating the generation of *hsa_circ_23897* and *hsa_circ_0049027* from its host gene, and validation by Sanger sequencing. d Real-time qRT-PCR assay showing the relative levels (normalized to β-actin) of *hsa_circ_23897* or *hsa_circ_0049027* in the peritumor and tumor tissues of gastric cancer (n = 81). e Dual-luciferase assay indicating the promoter activity of *HuR* in AGS and MKN-45 cells stably transfected with empty vector (*circ-Mock*), *hsa_circ-23897* (*circ_23897*), linear *circ-23897* (*lin_23897*), *circ-HuR*, or linear *circ-HuR* (*lin-HuR*). f and g Real-time qRT-PCR (f, normalized to β-actin, n = 5) and western blot (g) assays revealing the transcript and protein levels of *HuR* and its downstream target genes in AGS and MKN-45 cells stably transfected with *circ-Mock*, *circ-23897*, *lin_23897*, *circ-HuR*, or *lin-HuR*. h and i Western blot (h) and immunofluorescence (i) assays showing the cytoplasmic and nuclear accumulation of HuR in AGS and MKN-45 cells stably transfected with *circ-Mock*, *circ-HuR*, or *lin-HuR*. Nuclei were stained by DAPI (blue). Scale bar, 10 μm. j RNA-FISH assay indicating the nuclear localization of *circ-HuR* in AGS cells using an antisense probe (green), while sense probe was used as a negative control. U1 and *GAPDH* were applied as positive controls. Scale bar, 10 μm. Student’s t-test and ANOVA analyzed the difference in (d-f). *P < 0.01 vs. circ-Mock. Data are shown as mean ± SEM (error bars) and representative of three independent experiments in (a-c) and (e-j)

**Fig. 2**
Over-expression of *circ-HuR* suppresses the growth and aggressiveness of gastric cancer. a MTT colorimetric assay showing the viability of AGS and MKN-45 cells stably transfected with empty vector (*circ-Mock*), *circ-HuR*, or *lin-HuR*. b and c Soft agar (b) and matrigel invasion (c) assays indicating the in vitro growth and invasion of AGS and MKN-45 cells stably transfected with *circ-Mock*, *circ-HuR*, or *lin-HuR*. d Representative (left panel), in vivo growth curve (middle panel), and weight at the end points (right panel) of xenograft tumors formed by subcutaneous injection of AGS cells stably transfected with *circ-Mock* or *circ-HuR* into the dorsal flanks of nude mice (n = 5 for each group). e Representative images (left panel) and quantification (right panel) of immunohistochemical staining showing the expression of Ki-67 and CD31 within xenograft tumors formed by hypodermic injection of AGS cells stably transfected with *circ-Mock* or *circ-HuR* (n = 5 for each group). Scale bars: 50 μm. f-h Representative images (f), H&E staining (g, arrowheads), and quantification (h, left panel) of lung metastatic colonization and Kaplan-Meier curves (h, right panel) of nude mice treated with tail vein injection of AGS cells stably transfected with mock or *circ-HuR* (n = 5 for each group). Scale bar: 100 μm. ANOVA and Student’s t-test analyzed the difference in a-e and h. Log-rank test for survival comparison in (h). *P < 0.01 vs. circ-Mock. Data are shown as mean ± SEM (error bars) and representative of three independent experiments in (a-c)

**Fig. 3**
*Circ-HuR* interacts with CNBP protein in gastric cancer. a Coomassie bright blue staining (left panel), mass spectrometry (MS) assay, and overlapping analysis (Venn diagram, right panel) with established RBP and TF databases revealing the proteins pulled down by biotin-labeled linear or circular forms of *circ-HuR* from the lysates of AGS cells. b RIP and real-time qRT-PCR assays showing the relative interaction between *circ-HuR* and six proteins in AGS cells stably transfected with empty vector (*circ-Mock*), *hsa_circ-23897* (*circ_23897*), linear *circ-23897* (*lin_23897*), *circ-HuR*, or linear *circ-HuR* (*lin-HuR*), with normalization to input of cells transfected with *circ-Mock*. c RIP assay with primer sets (lower panel) indicating the interaction between *circ-HuR* and CNBP in AGS cells stably transfected with *circ-Mock*, *circ_23897*, *lin_23897*, *circ-HuR*, or *lin-HuR* (upper panel). d MS assay depicting the identified CNBP peptides pulled down by *circ-HuR*. e Dual RNA-FISH and immunofluorescence staining assay indicating the co-localization of *circ-HuR* (green) and CNBP (red) in AGS and MKN-45 cells, with nuclei staining with DAPI (blue). Scale bar, 5 μm. f RNA EMSA determining the interaction between endogenous CNBP protein and biotin-labeled circular probe of *circ-HuR* (arrowheads), with CNBP antibody incubation or competition using an excess of unlabeled circular probe of *circ-HuR*. g Schematic diagram revealing the domains of CNBP truncations. h In vitro binding assay showing the enriched *circ-HuR* levels detected by RT-PCR (lower panel) after incubation with full-length or truncations of Flag-tagged or GST-tagged recombinant CNBP protein validated by western blot (upper panel). ANOVA analyzed the difference in (b). *P < 0.01 vs. circ-Mock. Data are shown as mean ± SEM (error bars) and representative of three independent experiments in (b, c, e, f, and h)

**Fig. 4**
CNBP promotes *HuR* expression, growth, and aggressiveness of gastric cancer. a Schematic illustration of dCas9-based CRISPRi for *CNBP* and small guide RNA (sgRNA) targeting region. b Dual-luciferase assay revealing the promoter activity of *HuR* in AGS and MKN-45 cells stably transfected with empty vector (mock), *CNBP,* CRISPRi-Scb, CRISPRi-CNBP #1, or CRISPRi-CNBP #2. (c) and (d) Real-time qRT-PCR (c, normalized to β-actin, n = 5) and western blot (d) assays showing the transcript and protein levels of *HuR* in AGS and MKN-45 cells stably transfected with mock, *CNBP*, CRISPRi-Scb, CRISPRi-CNBP #1, or CRISPRi-CNBP #2. e MTT colorimetric assay indicating the viability of AGS and MKN-45 cells stably transfected with mock, *CNBP*, CRISPRi-Scb, or CRISPRi-CNBP #1. f and g Soft agar (f) and matrigel invasion (g) assays showing the in vitro growth and invasion of AGS and MKN-45 cells stably transfected with mock, *CNBP*, CRISPRi-Scb, or CRISPRi-CNBP #1. ANOVA analyzed the difference in (b, c and e-g). *P < 0.01 vs. mock or CRISPRi-Scb. Data are shown as mean ± SEM (error bars) and representative of three independent experiments in (b-g)

**Fig. 5**
*Circ-HuR* suppresses *HuR* expression, growth, and invasion of gastric cancer cells via repressing CNBP transactivation. a Dual-luciferase assay revealing the transactivation of CNBP in AGS and MKN-45 cells stably transfected with empty vector (mock) or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR*. b ChIP and qPCR assays showing the changes in binding of CNBP to *HuR* promoter in AGS and MKN-45 cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR*. c and d Dual-luciferase (c) and real-time qRT-PCR (d) assays indicating the activity of *HuR* promoter with wild type (WT) or mutant (Mut) CNBP binding site and transcript levels (normalized to β-actin, n = 4) of *HuR* in AGS and MKN-45 cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR*. e Western blot assay showing the expression of CNBP, HuR, CCND2, and CTNNB1 in AGS cells stably transfected with CRISPRi-Scb or CRISPRi-CNBP #1, and those co-transfected with mock, *CNBP*, *circ-Mock*, or *circ-HuR*. f MTT colorimetric assay indicating the viability of AGS and MKN-45 cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR*. g and h Soft agar (g) and matrigel invasion (h) assays showing in vitro growth and invasion of AGS and MKN-45 cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR*. ANOVA analyzed the difference in (a-d and f-h). *P < 0.01 vs. mock+ circ-Mock. Data are shown as mean ± SEM (error bars) and representative of three independent experiments in (a-h)

**Fig. 6**
*Circ-HuR* suppresses gastric cancer progression by inhibiting CNBP transactivation in vivo. a Representative (left panel), in vivo growth curve (middle panel), and weight at the end points (right panel) of xenograft tumors formed by subcutaneous injection of AGS cells stably transfected with empty vector (mock) or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR* into the dorsal flanks of nude mice (n = 5 for each group). b Representative images (left panel) and quantification (right panel) of immunohistochemical staining showing the expression of Ki-67 and CD31 within xenograft tumors formed by hypodermic injection of AGS cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR* (n = 5 for each group). Scale bars: 50 μm. c-e Representative images (c), H&E staining (d, arrowheads), and quantification (e, left panel) of lung metastatic colonization and Kaplan-Meier curves (e, right panel) of nude mice treated with tail vein injection of AGS cells stably transfected with mock or *CNBP*, and those co-transfected with *circ-Mock* or *circ-HuR* (n = 5 for each group). Scale bar: 100 μm. f The mechanisms underlying *circ-HuR*-suppressed tumor progression: as a nuclear circRNA, *circ-HuR* interacts with CNBP to inhibit its binding to *HuR* promoter, resulting in down-regulation of *HuR* and suppression of gastric cancer progression. ANOVA analyzed the difference in (a, b, e). Log-rank test for survival comparison in (e). *P < 0.01 vs. mock+ circ-Mock. Data are shown as mean ± SEM (error bars)

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References

1. Van Cutsem E, Sagaert X, Topal B, Haustermans K, Prenen H. Gastric cancer. Lancet. 2016;388:2654–2664. doi: 10.1016/S0140-6736(16)30354-3. - DOI - PubMed
1. Zucal C, D'Agostino V, Loffredo R, Mantelli B, NatthakanThongon LP, Latorre E, Provenzani A. Targeting the multifaceted HuR protein, benefits and caveats. Curr Drug Targets. 2015;16:499–515. doi: 10.2174/1389450116666150223163632. - DOI - PubMed
1. Doller A, el-S A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol. 2008;28:2608–2625. doi: 10.1128/MCB.01530-07. - DOI - PMC - PubMed
1. Vazquez-Chantada M, Fernandez-Ramos D, Embade N, Martinez-Lopez N, Varela-Rey M, Woodhoo A, Luka Z, Wagner C, Anglim PP, Finnell RH, et al. HuR/methyl-HuR and AUF1 regulate the MAT expressed during liver proliferation, differentiation, and carcinogenesis. Gastroenterology. 2010;138:1943–1953. doi: 10.1053/j.gastro.2010.01.032. - DOI - PMC - PubMed
1. Kotta-Loizou I, Giaginis C, Theocharis S. Clinical significance of HuR expression in human malignancy. Med Oncol. 2014;31:161. doi: 10.1007/s12032-014-0161-y. - DOI - PubMed

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[1] Van Cutsem E, Sagaert X, Topal B, Haustermans K, Prenen H. Gastric cancer. Lancet. 2016;388:2654–2664. doi: 10.1016/S0140-6736(16)30354-3. - DOI - PubMed

[2] Van Cutsem E, Sagaert X, Topal B, Haustermans K, Prenen H. Gastric cancer. Lancet. 2016;388:2654–2664. doi: 10.1016/S0140-6736(16)30354-3. - DOI - PubMed

[3] Zucal C, D'Agostino V, Loffredo R, Mantelli B, NatthakanThongon LP, Latorre E, Provenzani A. Targeting the multifaceted HuR protein, benefits and caveats. Curr Drug Targets. 2015;16:499–515. doi: 10.2174/1389450116666150223163632. - DOI - PubMed

[4] Zucal C, D'Agostino V, Loffredo R, Mantelli B, NatthakanThongon LP, Latorre E, Provenzani A. Targeting the multifaceted HuR protein, benefits and caveats. Curr Drug Targets. 2015;16:499–515. doi: 10.2174/1389450116666150223163632. - DOI - PubMed

[5] Doller A, el-S A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol. 2008;28:2608–2625. doi: 10.1128/MCB.01530-07. - DOI - PMC - PubMed

[6] Doller A, el-S A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, Eberhardt W. Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol. 2008;28:2608–2625. doi: 10.1128/MCB.01530-07. - DOI - PMC - PubMed

[7] Vazquez-Chantada M, Fernandez-Ramos D, Embade N, Martinez-Lopez N, Varela-Rey M, Woodhoo A, Luka Z, Wagner C, Anglim PP, Finnell RH, et al. HuR/methyl-HuR and AUF1 regulate the MAT expressed during liver proliferation, differentiation, and carcinogenesis. Gastroenterology. 2010;138:1943–1953. doi: 10.1053/j.gastro.2010.01.032. - DOI - PMC - PubMed

[8] Vazquez-Chantada M, Fernandez-Ramos D, Embade N, Martinez-Lopez N, Varela-Rey M, Woodhoo A, Luka Z, Wagner C, Anglim PP, Finnell RH, et al. HuR/methyl-HuR and AUF1 regulate the MAT expressed during liver proliferation, differentiation, and carcinogenesis. Gastroenterology. 2010;138:1943–1953. doi: 10.1053/j.gastro.2010.01.032. - DOI - PMC - PubMed

[9] Kotta-Loizou I, Giaginis C, Theocharis S. Clinical significance of HuR expression in human malignancy. Med Oncol. 2014;31:161. doi: 10.1007/s12032-014-0161-y. - DOI - PubMed

[10] Kotta-Loizou I, Giaginis C, Theocharis S. Clinical significance of HuR expression in human malignancy. Med Oncol. 2014;31:161. doi: 10.1007/s12032-014-0161-y. - DOI - PubMed

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Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation

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Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation

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